Prominent intraspecific genetic divergence within Anopheles gambiae sibling species triggered by habitat discontinuities across a riverine landscape

Molecular Ecology

Volumn 23, Issue 18, 2014, Pages 4574-4589

  Caputo, B ^a   Nwakanma, D ^b   Caputo, F P ^a   Jawara, M ^b   Oriero, E C ^b   Hamidadiamoh, M ^b   Dia, I ^c   Konate, L ^d   Petrarca, V ^e   Pinto, J ^f   Conway, D J ^b   Della Torre, A ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b MEDICAL RESEARCH COUNCIL LABORATORIES   (Gambia)

^c INSTITUT PASTEUR DE DAKAR   (Senegal)

^d UNIVERSITÉ CHEIKH ANTA DIOP   (Senegal)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

Author keywords

Genetics; Landscape; Molecular evolution; Mosquitoes; Parasitology; Population genetics empirical; Speciation

Indexed keywords

MICROSATELLITE DNA;

AFRICA; ANIMAL; ANOPHELES; ANOPHELES GAMBIAE; ARTICLE; BIOLOGICAL MODEL; CHROMOSOME INVERSION; ECOSYSTEM; GENE FLOW; GENETIC POLYMORPHISM; GENETICS; LANDSCAPE; MOLECULAR EVOLUTION; MOSQUITO; PARASITOLOGY; POPULATION GENETICS; POPULATION GENETICS-EMPIRICAL; RIVER; SPECIES DIFFERENTIATION; SYMPATRY;

GENETICS; LANDSCAPE; MOLECULAR EVOLUTION; MOSQUITOES; PARASITOLOGY; POPULATION GENETICS-EMPIRICAL; SPECIATION;

AFRICA, WESTERN; ANIMALS; ANOPHELES; ANOPHELES GAMBIAE; CHROMOSOME INVERSION; ECOSYSTEM; GENE FLOW; GENETIC SPECIATION; GENETICS, POPULATION; MICROSATELLITE REPEATS; MODELS, GENETIC; POLYMORPHISM, GENETIC; RIVERS; SYMPATRY;

EID: 84908143086     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12866     Document Type: Article

References (93)

1. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics, 9, 323.
2. Ashburner M, Carson HL, Thompson JN (1986) The Genetics and Biology of Drosophila, Vol. 3. Academic Press, London.
3. Ayala FJ, Coluzzi M (2005) Chromosome speciation: humans, Drosophila, and mosquitoes. Proceedings of the National Academic Sciences of the Unites States of America, 102, 6535-6542.
4. Ayala D, Fontaine MC, Cohuet A, Fontenille D, Vitalis R, Simard F (2011) Chromosomal inversions, natural selection and adaptation in the malaria vector Anopheles funestus. Molecular Biology and Evolution, 28, 745-758.
5. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London, Series B: Biological Sciences, 263, 1619-1626.
6. Bøgh C, Bøgh C, Clarke SE, Jawara M, Thomas CJ, Lindsay SW (2003) Localized breeding of the Anopheles gambiae complex (Diptera: Culicidae) along the River Gambia, West Africa. Bulletin of Entomological Research, 93, 279-287.
7. Boissiere A, Gimonneau G, Tchioffo MT et al. (2013) Application of a qPCR Assay in the Investigation of Susceptibility to Malaria Infection of the M and S Molecular Forms of An. gambiae s.s. in Cameroon. PLoS ONE, 8, e54820.
8. Bryan JH, Deco MAD, Petrarca V, Coluzzi M (1982) Inversion polymorphism and incipient speciation in Anopheles gambiae s.str in The Gambia, West Africa. Genetica, 59, 167-176.
9. Caputo B, Nwakanma D, Jawara M et al. (2008) Anopheles gambiae complex along The Gambia river, with particular reference to the molecular forms of An. gambiae s.s. Malaria Journal, 7, 182.
10. Caputo B, Santolamazza F, Vicente JL et al. (2011) The 'Far-West' of Anopheles gambiae molecular forms. PLoS ONE, 6, e16415.
11. Cassone BJ, Kamdem C, Cheng C et al. (2014) Gene expression divergence between malaria vector sibling species Anopheles gambiae and An. coluzzii from rural and urban Yaounde Cameroon. Molecular Ecology, 23, 2242-2259.
12. Chen C, Durand E, Forbes F, Francois O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Molecular Ecology Notes, 7, 747-756.
13. Coetzee M, Hunt RH, Wilkerson R, della Torre A, Coulibaly MB, Besansky NJ (2013) Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa, 3619, 246-274.
14. Coluzzi M (1982) Spatial distribution of chromosomal inversions and speciation in Anopheline mosquitoes. Progress in Clinical and Biological Research, 96, 143-153.
15. Coluzzi M, Petrarca V (1973) Aspirator with paper cup for collecting mosquitos and other insects. Mosquito News, 33, 249-250.
16. Coluzzi M, Sabatini A, Petrarca V, Di Deco MA (1977) Behavioural divergences between mosquitoes with different inversion karyotypes in polymorphic populations of the Anopheles gambiae complex. Nature, 266, 832-833.
17. Coluzzi M, Sabatini A, Petrarca V, Di Deco MA (1979) Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Transactions of the Royal Society of Tropical Medicine and Hygiene, 73, 483-497.
18. Coluzzi M, Petrarca V, di Deco MA (1985) Chromosomal inversion intergradation and incipient speciation in Anopheles gambiae. Bolletino di Zoologia, 52, 45-63.
19. Coluzzi M, Sabatini A, della Torre A, Deco MAD, Petrarca V (2002) A polytene chromosome analysis of the Anopheles gambiae species complex. Science, 298, 1415-1418.
20. Crispo E, Moore J-S, Lee-Yaw JA, Gray SM, Haller BC (2011) Broken barriers: human-induced changes to gene flow and introgression in animals. BioEssays, 33, 508-518.
21. Davidson G (1964) Anopheles gambiae, a complex of species. Bulletin of the World Health Organization, 31, 625-634.
22. Davidson G, Jackson CE (1962) Incipient speciation in Anopheles gambiae Giles. Bulletin of the World Health Organization, 27, 303-305.
23. Diabatle A, Dabirle RK, Heidenberger K et al. (2008) Evidence for divergent selection between the molecular forms of Anopheles gambiae: role of predation. BMC Evolutionary Biology, 8, 5.
24. Donnelly MJ, Cuamba N, Charlwood JD, Collins FH, Townson H (1999) Population structure in the malaria vector, Anopheles arabiensis patton in East Africa. Heredity (Edinb), 83, 408-417.
25. Donnelly MJ, Licht MC, Lehmann T (2001) Evidence for recent population expansion in the evolutionary history of the malaria vectors Anopheles arabiensis and Anopheles gambiae. Molecular Biology and Evolution, 18, 1353-1364.
26. Durand E, Jay F, Gaggiotti OE, Francois O (2009) Spatial inference of admixture proportions and secondary contact zones. Molecular Biology and Evolution, 26, 1963-1973.
27. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
28. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology, 14, 2611-2620.
29. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
30. Francois O, Ancelet S, Guillot G (2006) Bayesian clustering using hidden markov random fields in spatial population. Genetics, 174, 805-816.
31. Fryxell RT, Nieman CC, Fofana A et al. (2012) Differential Plasmodium falciparum infection of Anopheles gambiae s.s. molecular and chromosomal forms in Mali. Malaria Journal, 11, 133.
32. Garrigan D, Kingan SB, Geneva AJ et al. (2012) Genome sequencing reveals complex speciation in the Drosophila simulans clade. Genome Research, 22, 1499-1511.
33. Gimonneau G, Bouyer J, Morand S, Besansky NJ, Diabate A, Simard F (2010) A behavioral mechanism underlying ecological divergence in the malaria mosquito Anopheles gambiae. Behavioral Ecology, 21, 1087-1092.
34. Gimonneau G, Pombi M, Dabire RK, Diabate A, Morand S, Simard F (2012) Behavioural responses of Anopheles gambiae sensu stricto M and S molecular form larvae to an aquatic predator in Burkina Faso. Parasites and Vectors, 5, 65.
35. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9. 3).
36. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution, 59, 1633-1638.
37. Holm S (1979) A simple sequentially rejective multiple test procedure. Scandinavian journal of statistics, 6, 65-70.
38. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801-1806.
39. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics, 6, 13.
40. Kalinowski ST (2008) Treefit. A computer program for evaluating how well evolutionary trees fit genetic distance data.
41. Krzywinski J, Besansky NJ (2003) Molecular systematics of anopheles: from subgenera to subpopulations. Annual Review of Entomology, 48, 111-139.
42. Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE Jr (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conservation Genetics, 7, 295-302.
43. Lee Y, Cornel AJ, Meneses CR et al. (2009) Ecological and genetic relationships of the Forest-M form among chromosomal and molecular forms of the malaria vector Anopheles gambiae sensu stricto. Malaria Journal, 8, 75.
44. Lee Y, Marsden CD, Norris LC et al. (2013a) Spatiotemporal dynamics of gene flow and hybrid fitness between the M and S forms of the malaria mosquito, Anopheles gambiae. PNAS, 110, 19854-19859.
45. Lee Y, Collier TC, Sanford MR et al. (2013b) Chromosome inversions, genomic differentiation and speciation in the African malaria mosquito Anopheles gambiae. PLoS ONE, 8, e57887.
46. Legendre L, Legendre P (1983) Numerical ecology. Elsevier Available from: http://afrilib.odinafrica.org/handle/0/16235
47. Lehmann T, Diabate A (2008) The molecular forms of Anopheles gambiae: a phenotypic perspective. Infection, Genetics and Evolution, 8, 737-746.
48. Lehmann T, Hawley WA, Grebert H, Danga M, Atieli F, Collins FH (1999) The Rift Valley complex as a barrier to gene flow for Anopheles gambiae in Kenya. Journal of Heredity, 90, 613-621.
49. Lehmann T, Licht M, Elissa N et al. (2003) Population Structure of Anopheles gambiae in Africa. Journal of Heredity, 94, 133-147.
50. Li Z-M, Zheng X-M, Ge S (2011) Genetic diversity and domestication history of African rice (Oryza glaberrima) as inferred from multiple gene sequences. TAG. Theoretical and Applied Genetics., 123, 21-31.
51. Manoukis NC, Powell JR, Toure MB et al. (2008) A test of the chromosomal theory of ecotypic speciation in Anopheles gambiae. Proceedings of the National Academy of Sciences of the United States of America, 105, 2940-2945.
52. Marsden CD, Lee Y, Nieman CC et al. (2011) Asymmetric introgression between the M and S forms of the malaria vector, Anopheles gambiae, maintains divergence despite extensive hybridization. Molecular Ecology, 20, 4983-4994.
53. Martin SH, Dasmahapatra KK, Nadeau NJ et al. (2013) Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Research, 23, 1817-1828.
54. Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution, 60, 2399-2402.
55. Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Molecular Ecology Resources, 11, 5-18.
56. Michel AP, Ingrasci MJ, Schemerhorn BJ et al. (2005) Rangewide population genetic structure of the African malaria vector Anopheles funestus. Molecular Ecology, 14, 4235-4248.
57. Mousadik AE, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree Argania spinosa (L.) Skeels endemic to Morocco. Theoretical and Applied Genetics, 92, 832-839.
58. Nadeau NJ, Whibley A, Jones RT et al. (2012) Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Philosophical Transactions of the Royal Society B, 367, 343-353.
59. Ndiath MO, Cohuet A, Gaye A et al. (2011) Comparative susceptibility to Plasmodium falciparum of the molecular forms M and S of Anopheles gambiae and Anopheles arabiensis. Malaria Journal, 10, 269.
60. Ndjema? HN, Patchoke S, Atangana J et al. (2009) The distribution of insecticide resistance in Anopheles gambiae s.l populations from Cameroon: an update. Transactions of the Royal Society of Tropical Medicine and Hygiene, 103, 1127-1138.
61. Neafsey DE, Lawniczak MKN, Park DJ et al. (2010) SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science, 330, 514-517.
62. Nei M (1987) Molecular evolutionary genetics. Columbia University Press.
63. Nosil P, Harmon LJ, Seehausen O (2009) Ecological explanations for (incomplete) speciation. Trends in Ecology & Evolution, 24, 145-156.
64. Nwakanma DC, Neafsey DE, Jawara M et al. (2013) Breakdown in the process of incipient speciation in Anopheles gambiae. Genetics, 193, 1221-1231.
65. Oliveira E, Salgueiro P, Palsson K et al. (2008) High levels of hybridization between molecular forms of Anopheles gambiae from Guinea Bissau. Journal of medical entomology, 45, 1057-1063.
66. Petrarca V, Carrara GC, Di Deco MA, Petrangeli G (1983) The Anopheles gambiae complex in Guinea Bissau. Parassitologia, 25, 29-39.
67. Pinto J, Egyir-Yawson A, Vicente J et al. (2013) Geographic population structure of the African malaria vector Anopheles gambiae suggests a role for the forest-savannah biome transition as a barrier to gene flow. Evolutionary Applications, 6, 910-924.
68. Pombi M, Caputo B, Simard F et al. (2008) Chromosomal plasticity and evolutionary potential in the malaria vector Anopheles gambiae sensu stricto: insights from three decades of rare paracentric inversions. BMC Evolutionary Biology, 8, 309.
69. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
70. Quantum GIS (2011) Development Team, 2012. Quantum GIS Geographic Information System. Open Source Geospatial Foundation Project. URL:[http://qgis. osgeo. org].
71. Reidenbach KR, Neafsey DE, Costantini C et al. (2012) Patterns of genomic differentiation between ecologically differentiated M and S Forms of Anopheles gambiae in West and Central Africa. Genome Biology and Evolution, 4, 1202-1212.
72. Robert V, Petrarca V, Coluzzi M, Bouidin C, Carnevale P (1991) Etude des taux de parturite et d'infection du complexe Anopheles gambiae dans la riziere de la Vallee du Kou, Burkina Faso. In: Le Paludisme en Afrique de l'Ouest (eds Robert V, Chippaux JP, Diomande L et collaborateurs), pp. 17-36. ORSTOM Editions, France.
73. Rousset F (2008) genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8, 103-106.
74. Rundle HD, Nosil P (2005) Ecological speciation. Ecology Letters, 8, 336-352.
75. Santolamazza F, Mancini E, Simard F, Qi Y, Tu Z, della Torre A (2008) Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms. Malaria Journal, 7, 163.
76. Shafer ABA, Jochen B, Wolf W (2013) Widespread evidence for incipient ecological speciation: a meta-analysis of isolationby-ecology. Ecology Letters, 16, 940-950.
77. Slotman MA, Tripet F, Cornel AJ et al. (2006) Evidence for subdivision within the M molecular form of Anopheles gambiae. Molecular Ecology, 16, 639-649.
78. Stump AD, Shoener JA, Costantini C, Sagnon N, Besansky NJ (2005) Sex-linked differentiation between incipient species of Anopheles gambiae. Genetics, 169, 1509-1519.
79. della Torre A (1997) Polytene chromosome preparation from anopheline mosquitoes. In: The Molecular Biology of Insect Disease Vectors (eds Crampton JM, Beard CB, Louis C), pp. 329-336. Springer, Netherlands. Available from: http://link. springer.com/chapter/10.1007/978-94-009-1535-0-28 della
80. Torre A, Fanello C, Akogbeto M et al. (2001) Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. Insect Molecular Biology, 10, 9-18.
81. della Torre A, Tu Z, Petrarca V (2005) On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. Insect Biochemistry and Molecular Biology, 35, 755-769.
82. Toure YT, Petrarca V, Traore SF et al. (1994) Ecological genetic studies in the chromosomal form Mopti of Anopheles gambiae s.str in Mali, west Africa. Genetica, 94, 213-223.
83. Toure YT, Petrarca V, Traore SF 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.
84. Turner TL, Hahn MW, Nuzhdin SV (2005) Genomic islands of speciation in Anopheles gambiae. PLoS Biology, 3, e285.
85. Wang R, Kafatos FC, Zheng L (1999) Microsatellite markers and genotyping procedures for Anopheles gambiae. Parasitology Today, 15, 33-37.
86. Wang-Sattler R, Blandin S, Ning Y et al. (2007) Mosaic genome architecture of the Anopheles gambiae species complex. PLoS ONE, 2, e1249.
87. Weetman D, Wilding CS, Steen K, Pinto J, Donnelly MJ (2012) Gene flow-dependent genomic divergence between Anopheles gambiae M and S Forms. Molecular Biology and Evolution, 29, 279-291.
88. Weir BS, Cockerham CC (1984) Estimating F-Statistics for the analysis of population structure. Evolution, 38, 1358.
89. White BJ, Lawniczak MKN, Cheng C et al. (2011) Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium. PNAS, 108, 244-249.
90. Wondji C, Simard F, Petrarca V et al. (2005) Species and populations of the Anopheles gambiae complex in Cameroon with special emphasis on chromosomal and molecular forms of Anopheles gambiae s.s. Journal of Medical Entomology, 42, 998-1005.
91. Wood SA (2013) The Gambia river. In: Biomes and Ecosystems: An Encyclopedia (ed. Howarth RW), pp. 584-586. Salem Press, Ipswich, Massachusetts.
92. Yawson AE, Weetman D, Wilson MD, Donnelly MJ (2007) Ecological zones rather than molecular forms predict genetic differentiation in the malaria vector Anopheles gambiae s.s. in Ghana. Genetics, 175, 751-761.
93. Zheng L, Benedict MQ, Cornel AJ, Collins FH, Kafatos FC (1996) An integrated genetic map of the African human malaria vector mosquito, Anopheles gambiae. Genetics, 143, 941-952.