Centromere-proximal differentiation and speciation in Anopheles gambiae - PubMed (original) (raw)
Centromere-proximal differentiation and speciation in Anopheles gambiae
Aram D Stump et al. Proc Natl Acad Sci U S A. 2005.
Abstract
The M and S molecular forms of Anopheles gambiae are undergoing speciation as they adapt to heterogeneities in the environment, spreading malaria in the process. We hypothesized that their divergence despite gene flow is facilitated by reduced recombination at the centromeric (proximal) end of the X chromosome. We sequenced introns from 22 X chromosome genes in M and S from two locations of West Africa where the forms are sympatric. Generally, in both forms nucleotide diversity was high distally, lower proximally, and very low nearest the centromere. Conversely, differentiation between the forms was virtually zero distally and very high proximally. Pairwise comparisons to a close relative, the sibling species Anopheles arabiensis, demonstrated uniformly high divergence regardless of position along the X chromosome, suggesting that this pattern is not purely mechanical. Instead, the pattern observed for M and S suggests the action of divergent natural selection countering gene flow only at the proximal end of the X chromosome, where recombination is reduced. Comparison of sites with fixed differences between M and S to the corresponding sites in A. arabiensis revealed that derived substitutions had been fixed in both forms, further supporting the hypothesis that both have been under selection. These derived substitutions are fixed in the two West African samples and in samples of S from western and coastal Kenya, suggesting that selection occurred before the forms expanded to their current ranges. Our findings are consistent with a role for suppressed genetic recombination in speciation of A. gambiae.
Figures
Fig. 1.
Relative location of loci on a cytogenetic map of the A. gambiae X chromosome, oriented with the centromere on the right. Numbering of divisions and subdivisions is relative to an arbitrary chromosomally standard reference (33).
Fig. 2.
Polymorphism and divergence in West African samples of A. gambiae M and S. The x axis showing the loci that were surveyed is not drawn to scale. (A) Nucleotide diversity. Error bars indicate one standard deviation. (B) Differentiation. Asterisks indicate significant _F_ST values after Bonferroni correction. (C) Proportion of fixed differences and shared or exclusive polymorphisms. Polymorphisms include insertion/deletions.
Similar articles
- SINE insertion polymorphism on the X chromosome differentiates Anopheles gambiae molecular forms.
Barnes MJ, Lobo NF, Coulibaly MB, Sagnon NF, Costantini C, Besansky NJ. Barnes MJ, et al. Insect Mol Biol. 2005 Aug;14(4):353-63. doi: 10.1111/j.1365-2583.2005.00566.x. Insect Mol Biol. 2005. PMID: 16033429 - Variation in recombination rate across the X chromosome of Anopheles gambiae.
Pombi M, Stump AD, Della Torre A, Besansky NJ. Pombi M, et al. Am J Trop Med Hyg. 2006 Nov;75(5):901-3. Am J Trop Med Hyg. 2006. PMID: 17123984 - Sex-linked differentiation between incipient species of Anopheles gambiae.
Stump AD, Shoener JA, Costantini C, Sagnon N, Besansky NJ. Stump AD, et al. Genetics. 2005 Mar;169(3):1509-19. doi: 10.1534/genetics.104.035303. Epub 2005 Jan 16. Genetics. 2005. PMID: 15654109 Free PMC article. - Evidence for X-linked introgression between molecular forms of Anopheles gambiae from Angola.
Choi KS, Townson H. Choi KS, et al. Med Vet Entomol. 2012 Jun;26(2):218-27. doi: 10.1111/j.1365-2915.2011.00977.x. Epub 2011 Sep 20. Med Vet Entomol. 2012. PMID: 21933220 - Population structure, speciation, and introgression in the Anopheles gambiae complex.
Powell JR, Petrarca V, della Torre A, Caccone A, Coluzzi M. Powell JR, et al. Parassitologia. 1999 Sep;41(1-3):101-13. Parassitologia. 1999. PMID: 10697841 Review.
Cited by
- Male-biased recombination at chromosome ends in a songbird revealed by precisely mapping crossover positions.
Zhang H, Lundberg M, Ponnikas S, Hasselquist D, Hansson B. Zhang H, et al. G3 (Bethesda). 2024 Sep 4;14(9):jkae150. doi: 10.1093/g3journal/jkae150. G3 (Bethesda). 2024. PMID: 38985659 Free PMC article. - Lacustrine speciation associated with chromosomal inversion in a lineage of riverine fishes.
MacGuigan DJ, Krabbenhoft TJ, Harrington RC, Wainwright DK, Backenstose NJC, Near TJ. MacGuigan DJ, et al. Evolution. 2023 Jun 29;77(7):1505-1521. doi: 10.1093/evolut/qpad067. Evolution. 2023. PMID: 37094800 Free PMC article. - Molecular characterization and genetic authentication assay for Anopheles 'hemocyte-like' cell lines 4a-3A and 4a-3B.
Eggleston H, Njoya K, Anderson CE, Holm I, Eiglmeier K, Liang J, Sharakhov IV, Vernick KD, Riehle MM. Eggleston H, et al. Parasit Vectors. 2022 Dec 13;15(1):465. doi: 10.1186/s13071-022-05590-3. Parasit Vectors. 2022. PMID: 36514125 Free PMC article. - Anopheles gambiae Genome Conservation as a Resource for Rational Gene Drive Target Site Selection.
Kranjc N, Crisanti A, Nolan T, Bernardini F. Kranjc N, et al. Insects. 2021 Jan 23;12(2):97. doi: 10.3390/insects12020097. Insects. 2021. PMID: 33498790 Free PMC article. - High-resolution transcriptional profiling of Anopheles gambiae spermatogenesis reveals mechanisms of sex chromosome regulation.
Taxiarchi C, Kranjc N, Kriezis A, Kyrou K, Bernardini F, Russell S, Nolan T, Crisanti A, Galizi R. Taxiarchi C, et al. Sci Rep. 2019 Oct 16;9(1):14841. doi: 10.1038/s41598-019-51181-1. Sci Rep. 2019. PMID: 31619757 Free PMC article.
References
- Ortiz-Barrientos, D., Reiland, J., Hey, J. & Noor, M. A. (2002) Genetica 116, 167-178. - PubMed
- Butlin, R. K. (2005) Mol. Ecol. 14, 2621-2635. - PubMed
- Rieseberg, L. H. (2001) Trends Ecol. Evol. 16, 351-358. - PubMed
- Navarro, A. & Barton, N. H. (2003) Science 300, 321-324. - PubMed
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources