No evidence for biased co-transmission of speciation Islands in anopheles gambiae

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1587, 2012, Pages 374-384

  Hahn, Matthew W ^a   White, Bradley J ^b   Muir, Christopher D ^a   Besansky, Nora J ^b  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

Anopheles gambiae; Centromeric drive; Speciation

Indexed keywords

ALLELE; DIVERGENCE; EVOLUTIONARY BIOLOGY; GENE FLOW; GENOMICS; GENOTYPE; HIERARCHICAL SYSTEM; INTROGRESSION; MOSQUITO; PROBABILITY; SPECIATION (BIOLOGY);

EID: 84255162310     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0188     Document Type: Article

References (66)

1. Nosil, P., Funk, D. J. & Ortiz-Barrientos, D. 2009 Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18, 375-402. (doi:10.1111/j.1365-294X.2008.03946.x)
2. 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)
3. Wu, C. I. 2001 The genic view of the process of speciation. J. Evol. Biol. 14, 851-865. (doi:10.1046/j.1420-9101.2001.00335.x)
4. Wu, C. I. & Ting, C. T. 2004 Genes and speciation. Nat. Rev. Genet. 5, 114-122. (doi:10.1038/nrg1269)
5. Barton, N. H. 2006 Evolutionary biology: how did the human species form? Curr. Biol. 16, R647-R650. (doi:10.1016/j.cub.2006.07.032)
6. Wakeley, J. 2008. Complex speciation of humans and chimpanzees. Nature 452, E3-E4. (doi:10.1038/nature06805)
7. Turner, T. L. & Hahn, M. W. 2010 Genomics islands of speciation or genomics islands and speciation? Mol. Ecol. 19, 848-850. (doi:10.1111/j.1365-294X.2010.04532.x)
8. White, B. J., Cheng, C. D., Simard, F., Costantini, C. & Besansky, N. J. 2010 Genetic association of physically unlinked islands of genomic divergence in incipient species of Anopheles gambiae. Mol. Ecol. 19, 925-939. (doi:10.1111/j.1365-294X.2010.04531.x)
9. Barton, N. & Bengtsson, B. O. 1986 The barrier to genetic exchange between hybridizing populations. Heredity 57, 357-376. (doi:10.1038/hdy.1986.135)
10. Harrison, R. G. 1990 Hybrid zones: windows on evolutionary processes. In Oxford surveys in evolutionary biology (eds J. Antonovics & D. Futuyma), pp. 69-128. Oxford, UK: Oxford University Press.
11. Rieseberg, L. H., Whitton, J. & Gardner, K. 1999 Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152, 713-727.
12. Gompert, Z., Parchman, T. L. & Buerkle, C. A. 2012 Genomics of isolation in hybrids. Phil. Trans. R. Soc. B 367, 439-450. (doi:10.1098/rstb.2011.0196)
13. Payseur, B. A., Krenz, J. G. & Nachman, M. W. 2004 Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58, 2064-2078.
14. Teeter, K. C. et al. 2008 Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res. 18, 67-76. (doi:10.1101/gr.6757907)
15. Geraldes, A., Ferrand, N. & Nachman, M.W. 2006 Contrasting patterns of introgression at X-linked loci across the hybrid zone between subspecies of the European rabbit (Oryctolagus cuniculus). Genetics 173, 919-933. (doi:10.1534/genetics.105.054106)
16. Baxter, S. W. et al. 2010 Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. PLoS Genet. 6, e1000794. (doi:10.1371/journal.pgen.1000794)
17. Counterman, B. A. et al. 2010 Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in Heliconius erato. PLoS Genet. 6, e1000796. (doi:10.1371/journal.pgen.1000796)
18. Kronforst, M. R., Young, L. G., Blume, L. M. & Gilbert, L. E. 2006 Multilocus analyses of admixture and introgression among hybridizing Heliconius butterflies. Evolution 60, 1254-1268.
19. Nadeau, N. J. et al. 2012 Genomic islands of divergence in hybridizing Heliconius butterflies identified by largescale targeted sequencing. Phil. Trans. R. Soc. B 367, 343-353. (doi:10.1098/rstb.2011.0198)
20. dellaTorre, A., Fanello, C., Akogbeto, M., Dossou-yovo, J., Favia, G., Petrarca, V. & Coluzzi, M. 2001 Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. Insect Mol. Biol. 10, 9-18. (doi:10.1046/j.1365-2583.2001.00235.x)
21. Favia, G., Lanfrancotti, A., Spanos, L., Siden-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. (doi:10.1046/j.1365-2583.2001.00236.x)
22. Gentile, G., Slotman, M., Ketmaier, V., Powell, J. R. & Caccone, A. 2001 Attempts to molecularly distinguish cryptic taxa in Anopheles gambiae s.s. Insect Mol. Biol. 10, 25-32. (doi:10.1046/j.1365-2583.2001.00237.x)
23. della Torre, A., Tu, Z. & Petrarca, V. 2005 On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. Insect Biochem. Mol. Biol. 35, 755-769. (doi:10.1016/j.ibmb.2005.02.006)
24. Lehmann, T. & Diabate, A. 2008 The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect. Genet. Evol. 8, 737-746. (doi:10.1016/j.meegid.2008.06.003)
25. della Torre, A., Costantini, C., Besansky, N. J., Caccone, A., Petrarca, V., Powell, J. R. & Coluzzi, M. 2002 Speciation within Anopheles gambiae-the glass is half full. Science 298, 115-117. (doi:10.1126/science.1078170)
26. Crawford, J. E. & Lazzaro, B. P. 2010 The demographic histories of the M and S molecular forms of Anopheles gambiae s.s. Mol. Biol. Evol. 27, 1739-1744. (doi:10.1093/molbev/msq070)
27. Diabate, A. et al. 2005 Larval development of the molecular forms of Anopheles gambiae (Diptera: Culicidae) in different habitats: a transplantation experiment. J. Med. Entomol. 42, 548-553. (doi:10.1603/0022-2585(2005)042[0548:LDOTMF]2.0.CO;2)
28. Diabate, A., Dabire, R.K., Heidenberger, K., Crawford, J., Lamp, W. O., Culler, L. E. & Lehmann, T. 2008 Evidence for divergent selection between the molecular forms of Anopheles gambiae: role of predation. BMC Evol. Biol. 8, 5. (doi:10.1186/1471-2148-8-5)
29. Diabate, A., Dao, A., Yaro, A. S., Adamou, A., Gonzalez, R., Manoukis, N. C., Traore, S. F., Gwadz, R. W. & Lehmann, T. 2009 Spatial swarm segregation and reproductive isolation between the molecular forms of Anopheles gambiae. Proc. R. Soc. B 276, 4215-4222. (doi:10.1098/rspb.2009.1167)
30. Tripet, F., Toure, Y. T., Taylor, C. E., Norris, D. E., Dolo, G. & Lanzaro, G. C. 2001 DNA analysis of transferred sperm reveals significant levels of gene flow between molecular forms of Anopheles gambiae. Mol. Ecol. 10, 1725-1732. (doi:10.1046/j.0962-1083.2001.01301.x)
31. Pennetier, C., Warren, B., Dabire, K. R., Russell, I. J. & Gibson, G. 2010 'Singing on the wing' as a mechanism for species recognition in the malarial mosquito Anopheles gambiae. Curr. Biol. 20, 131-136. (doi:10.1016/j.cub.2009.11.040)
32. Stump, A. D., Fitzpatrick, M. C., Lobo, N. F., Traore, S., Sagnon, N. F., Costantini, C., Collins, F. H. & Besansky, N. J. 2005 Centromere-proximal differentiation and speciation in Anopheles gambiae. Proc. Natl Acad. Sci. USA 102, 15930-15935. (doi:10.1073/pnas.0508161102)
33. 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. (doi:10.1093/molbev/msm143)
34. Lawniczak, M. K. N. et al. 2010 Widespread islands of divergence in Anopheles gambiae revealed by whole genome sequences. Science 330, 512-514. (doi:10.1126/science.1195755)
35. Neafsey, D. E. et al. 2010 Complex gene flow boundaries among sympatric Anopheles vector mosquito populations revealed by genome-wide SNP genotyping. Science 330, 514-517. (doi:10.1126/science.1193036)
36. Lanzaro, G. C., Toure, Y. T., Carnahan, J., Zheng, L. B., Dolo, G., Traore, S., Petrarca, V., Vernick, K. D. & Taylor, C. E. 1998 Complexities in the genetic structure of Anopheles gambiae populations in west Africa as revealed by microsatellite DNA analysis. Proc. Natl Acad. Sci. USA 95, 14260-14265. (doi:10.1073/pnas.95.24.14260)
37. Wang, R., Zheng, L. B., Toure, Y. T., Dandekar, T. & Kafatos, F. C. 2001 When genetic distance matters: measuring genetic differentiation at microsatellite loci in whole-genome scans of recent and incipient mosquito species. Proc. Natl Acad. Sci. USA 98, 10769-10774. (doi:10.1073/pnas.191003598)
38. Wondji, C., Simard, F. & Fontenille, D. 2002 Evidence for genetic differentiation between the molecular forms M and S within the forest chromosomal form of Anopheles gambiae in an area of sympatry. Insect Mol. Biol. 11, 11-19. (doi:10.1046/j.0962-1075.2001.00306.x)
39. Costantini, C. et al. 2009 Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecol. 9, 16. (doi:10.1186/1472-6785-9-16)
40. Gentile, G., della Torre, A., Maegga, B., Powell, J. R. & Caccone, A. 2002 Genetic differentiation in the African malaria vector, Anopheles gambiae ss, and the problem of taxonomic status. Genetics 161, 1561-1578.
41. Simard, F. et al. 2009 Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecol. 9, 17. (doi:10.1186/1472-6785-9-17)
42. Felsenstein, J. 1981 Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35, 124-138. (doi:10.2307/2407946)
43. Henikoff, S., Ahmad, K. & Malik, H. S. 2001 The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293, 1098-1102. (doi:10.1126/science.1062939)
44. Henikoff, S. & Malik, H. S. 2002 Selfish drivers. Nature 417, 227. (doi:10.1038/417227a)
45. Lee, C. E. & Frost, B. W. 2002 Morphological stasis in the Eurytemora affinis species complex (Copepoda: Temoridae). Hydrobiologia 480, 111-128. (doi:10.1023/A:1021293203512)
46. Fanello, C., Santolamazza, F. & della Torre, A. 2002 Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med. Vet. Entomol. 16, 461-464. (doi:10.1046/j.1365-2915.2002.00393.x)
47. Guo, Z., Liu, Q. H. & Smith, L. M. 1997 Enhanced discrimination of single nucleotide polymorphisms by artificial mismatch hybridization. Nat. Biotechnol. 15, 331-335. (doi:10.1038/nbt0497-331)
48. Wilkins, E. E., Howell, P. I. & Benedict, M. Q. 2006 IMP PCR primers detect single nucleotide polymorphisms for Anopheles gambiae species identification, Mopti and Savanna rDNA types, and resistance to dieldrin in Anopheles arabiensis. Malaria J. 5, 125. (doi:10.1186/1475-2875-5-125)
49. Santolamazza, F., della Torre, A. & Caccone, A. 2004 Short report: a new polymerase chain reaction-restriction fragment length polymorphism method to identify Anopheles arabiensis from An. gambiae and its two molecular forms from degraded DNA templates or museum samples. Am. J. Trop. Med. Hyg. 70, 604-606.
50. Burnham, K. P. & Anderson, D. R. 2002 Model selection and multimodel inference: a practical information-theoretic approach. New York, NY: Springer.
51. Fishman, L. & Saunders, A. 2008 Centromere-associated female meiotic drive entails male fitness costs in monkey flowers. Science 322, 1559-1562. (doi:10.1126/science.1161406)
52. Case, A. L. & Willis, J. H. 2008 Hybrid male sterility in Mimulus (Phrymaceae) is associated with a geographically restricted mitochondrial rearrangement. Evolution 62, 1026-1039. (doi:10.1111/j.1558-5646.2008.00360.x)
53. Fishman, L. & Willis, J. H. 2006 A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution 60, 1372-1381.
54. Sweigart, A. L., Fishman, L. & Willis, J. H. 2006 A simple genetic incompatibility causes hybrid male sterility in Mimulus. Genetics 172, 2465-2479. (doi:10.1534/genetics.105.053686)
55. Diabate, A., Dabire, R. K., Millogo, N. & Lehmann, T. 2007 Evaluating the effect of postmating isolation between molecular forms of Anopheles gambiae (Diptera: Culicidae). J. Med. Entomol. 44, 60-64. (doi:10.1603/0022-2585(2007)44[60:ETEOPI]2.0.CO;2)
56. Gimonneau, G., Bouyer, J., Morand, S., Besansky, N. J., Diabate, A. & Simard, F. 2010 A behavioral mechanism underlying ecological divergence in the malaria mosquito Anopheles gambiae. Behav. Ecol. 21, 1087-1092. (doi:10.1093/beheco/arq114)
57. Edillo, F. E., Toure, Y. T., Lanzaro, G. C., Dolo, G. & Taylor, C. E. 2002 Spatial and habitat distribution of Anopheles gambiae and Anopheles arabiensis (Diptera: Culicidae) in Banambani Village, Mali. J. Med. Entomol. 39, 70-77. (doi:10.1603/0022-2585-39.1.70)
58. Djogbenou, L., Chandre, F., Berthomieu, A., Dabire, R., Koffi, A., Alout, H. & Weill, M. 2008 Evidence of introgression of the ace-1R mutation and of the ace-1 duplication in West African Anopheles gambiae s. s. PLoS ONE 3, e2172. (doi:10.1371/journal.pone.0002172)
59. Etang, J. et al. 2009 Polymorphism of intron-1 in the voltage-gated sodium channel gene of Anopheles gambiae s.s. populations from Cameroon with emphasis on insecticide knockdown resistance mutations. Mol. Ecol. 18, 3076-3086. (doi:10.1111/j.1365-294X.2009.04256.x)
60. White, B. J. et al. 2011 Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium. Proc. Natl Acad. Sci. USA 108, 244-249. (doi:10.1073/pnas.1013648108)
61. Noor, M. A. F. & Bennett, S. M. 2009 Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 103, 439-444. (doi:10.1038/hdy.2009.151)
62. Pombi, M., Stump, A. D., della Torre, A. & Besansky, N. J. 2006 Variation in recombination rate across the X chromosome of Anopheles gambiae. Am. J. Trop. Med. Hyg. 75, 901-903.
63. Coluzzi, M., Sabatini, A., della Torre, A., Di Deco, M. A. & Petrarca, V. 2002 A polytene chromosome analysis of the Anopheles gambiae species complex. Science 298, 1415-1418. (doi:10.1126/science.1077769)
64. Cassone, B. J., Mouline, K., Hahn, M. W., Pombi, M., Simard, F., Costantini, C. & Besansky, N. J. 2008 Differential gene expression in incipient species of Anopheles gambiae. Mol. Ecol. 17, 2491-2504. (doi:10.1111/j.1365-294X.2008.03774.x)
65. Hey, J. & Nielsen, R. 2004 Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167, 747-760. (doi:10.1534/genetics.103.024182)
66. Hey, J. & Nielsen, R. 2007 Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc. Natl Acad. Sci. USA 104, 2785-2790. (doi:10.1073/pnas.0611164104)