Genetic association of physically unlinked islands of genomic divergence in incipient species of Anopheles gambiae

Abstract

Previous efforts to uncover the genetic underpinnings of ongoing ecological speciation of the M and S forms of the African malaria vector Anopheles gambiae revealed two centromere-proximal islands of genetic divergence on X and chromosome 2. Under the assumption of considerable ongoing gene flow between M and S, these persistently divergent genomic islands were widely considered to be “speciation islands”. In the course of microarray-based divergence mapping, we discovered a third centromere-associated island of divergence on chromosome 3, which was validated by targeted re-sequencing. To test for genetic association between the divergence islands on all three chromosomes, SNP-based assays were applied in four natural populations of M and S spanning West, Central and East Africa. Genotyping of 517 female M and S mosquitoes revealed nearly complete linkage disequilibrium between the centromeres of the three independently assorting chromosomes. These results suggest that despite the potential for inter-form gene flow through hybridization, actual (realized) gene flow between M and S may be substantially less than commonly assumed, and may not explain most shared variation. Moreover, the possibility of very low gene flow calls into question whether diverged pericentromeric regions-- characterized by reduced levels of variation and recombination-- are in fact instrumental rather than merely incidental to the speciation process.

Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium

“…We used a gene-based oligonucleotide microarray with a density of approximately one marker every 2 kb to map divergence between M and S. Using 10 sympatric M-and S-form mosquitoes sampled from Mali, we identified four regions of significantly elevated differentiation on homosequential chromosome arms, three of which were adjacent to centromeres on chromosomes X, 2, and 3 (14). The imputation of pericentromeric genes in reproductive or ecological isolation between M and S is complicated by low sequence diversity and reduced recombination characteristic of centromere-proximal regions (14,15), prompting us to concentrate follow-up effort on the fourth region, encompassing ∼100 kb on chromosome arm 3L, ∼11 Mb from the centromere (Fig.…”

“…The imputation of pericentromeric genes in reproductive or ecological isolation between M and S is complicated by low sequence diversity and reduced recombination characteristic of centromere-proximal regions (14,15), prompting us to concentrate follow-up effort on the fourth region, encompassing ∼100 kb on chromosome arm 3L, ∼11 Mb from the centromere (Fig. 1).…”

“…arabiensis. A maximum-likelihood implementation of the HKA test was performed using maximum-likelihood (ML) HKA (21) as described (14). Amino acid alignment was performed using MUSCLE.…”

A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks

“…One of the most controversial issues, from both theoretical expectations and empirical results, is the creation and maintenance/ growth of the genomic regions of divergence during speciation with gene flow (Hoffmann and Rieseberg, 2008;Feder and Nosil, 2010;White et al, 2010;Yeaman and Whitlock, 2011;Nachman and Payseur, 2012;Nosil and Feder, 2012;Feder et al, 2012b;Narum et al, 2013). Via (2009Via ( , 2012, proposed that strong divergent selection acting on a few loci generates an inter-population process, which she called divergence hitchhiking (DH), that is characterized by reduced inter-population recombination and gene flow.…”

Spatiotemporal dynamics of gene flow and hybrid fitness between the M and S forms of the malaria mosquito, Anopheles gambiae

“…A number of genomewide scans comparing M and S have been conducted since. These have applied several methods, including the same microarray used by Turner et al (25,26), high-density SNP arrays (12,21,23,27), and whole-genome sequencing (28). These studies likewise revealed little divergence except in a few discrete regions of the genome characterized by high levels of differentiation (islands of divergence).…”