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Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation.

Aboagye-Antwi F, Alhafez N, Weedall GD, Brothwood J, Kandola S, Paton D, Fofana A, Olohan L, Betancourth MP, Ekechukwu NE, Baeshen R, Traorè SF, Diabate A, Tripet F - PLoS Genet. (2015)

Bottom Line: Furthermore, full-genome sequencing confirmed that protein-coding differences between recombinant strains were limited to the experimentally swapped pericentromeric region.Finally, targeted-genome comparisons showed that a number of these unique differences were conserved in sympatric field populations, thereby revealing candidate speciation genes.The functional demonstration of a close association between speciation genes and the X-island of differentiation lends unprecedented support to island-of-speciation models of sympatric speciation facilitated by pericentric recombination suppression.

View Article: PubMed Central - PubMed

Affiliation: Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, United Kingdom; Department of Animal Biology and Conservation Science, Faculty of Sciences, University of Ghana, Legon, Ghana.

ABSTRACT
Although many theoretical models of sympatric speciation propose that genes responsible for assortative mating amongst incipient species should be associated with genomic regions protected from recombination, there are few data to support this theory. The malaria mosquito, Anopheles gambiae, is known for its sympatric cryptic species maintained by pre-mating reproductive isolation and its putative genomic islands of speciation, and is therefore an ideal model system for studying the genomic signature associated with incipient sympatric speciation. Here we selectively introgressed the island of divergence located in the pericentric region of the X chromosome of An. gambiae s.s. into its sister taxon An. coluzzii through 5 generations of backcrossing followed by two generations of crosses within the introgressed strains that resulted in An. coluzzii-like recombinant strains fixed for the M and S marker in the X chromosome island. The mating preference of recombinant strains was then tested by giving virgin recombinant individuals a choice of mates with X-islands matching and non-matching their own island type. We show through genetic analyses of transferred sperm that recombinant females consistently mated with matching island-type males thereby associating assortative mating genes with the X-island of divergence. Furthermore, full-genome sequencing confirmed that protein-coding differences between recombinant strains were limited to the experimentally swapped pericentromeric region. Finally, targeted-genome comparisons showed that a number of these unique differences were conserved in sympatric field populations, thereby revealing candidate speciation genes. The functional demonstration of a close association between speciation genes and the X-island of differentiation lends unprecedented support to island-of-speciation models of sympatric speciation facilitated by pericentric recombination suppression.

No MeSH data available.


Related in: MedlinePlus

Genomic structure of recombinant strains.The genomes of the assortatively-mating RbMM, RbSS and parental Mopti strains were compared using FST estimates at ~3x106 SNP marker loci (left Y-axis and red, blue and black lines). The genomic region introgressed from Kisumu into the Mopti genetic background and differing between the RbMM and RbSS recombinant strains is characterized by high FST values (blue shade) and extends from position ~14.5Mb to the centromere on chromosome X. The RbMM and RbSS differed at 160 protein-changing positions all of which located within the introgressed island and flanking region (right Y-axis, grey histogram bars). The pericentromeric region sharing conserved fixed differences with the field Anopheles coluzzii and gambiae s.s populations starts at position ~18.1Mb (orange shade). The position of inversions c, u and a on chromosome 2 is indicated (pink shade).
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pgen.1005141.g002: Genomic structure of recombinant strains.The genomes of the assortatively-mating RbMM, RbSS and parental Mopti strains were compared using FST estimates at ~3x106 SNP marker loci (left Y-axis and red, blue and black lines). The genomic region introgressed from Kisumu into the Mopti genetic background and differing between the RbMM and RbSS recombinant strains is characterized by high FST values (blue shade) and extends from position ~14.5Mb to the centromere on chromosome X. The RbMM and RbSS differed at 160 protein-changing positions all of which located within the introgressed island and flanking region (right Y-axis, grey histogram bars). The pericentromeric region sharing conserved fixed differences with the field Anopheles coluzzii and gambiae s.s populations starts at position ~18.1Mb (orange shade). The position of inversions c, u and a on chromosome 2 is indicated (pink shade).

Mentions: The size of the X-island of divergence and flanking regions differing between the RbMM and RbSS strains was determined through genome-wide genetic differentiation (FST) scans and the occurrence of fixed coding differences between the recombinant strains. Estimates of genetic differentiation between the RbMM, RbSS and Mopti strains were calculated for 3,743,318 SNPs across the X, 2nd and 3rd chromosomes. The genome-wide FST scans showed that the RbSS differs from the RbMM and Mopti strains on chromosome X from the centromere to the reference position ~14.8Mb (Fig 2). This region covered the entire island of speciation plus a large flanking region. In addition, the RbSS and RbMM strain were genetically differentiated at a ~2Mb S-form fragment extending roughly from positions 11.5–13.5Mb (Fig 2). There were no other sizeable S-like regions detected through comparisons of the RbMM, RbSS and Mopti genomes, indicating that the selective introgression design worked as hoped for. Importantly, amongst all fixed differences observed between the RbMM and RbSS strains, non-synonymous differences inducing protein-coding changes (n = 160) were found only in the selectively-introgressed pericentromeric region (Fig 2). Fixed differences located elsewhere in the genome were either coding synonymous changes or non-coding.


Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation.

Aboagye-Antwi F, Alhafez N, Weedall GD, Brothwood J, Kandola S, Paton D, Fofana A, Olohan L, Betancourth MP, Ekechukwu NE, Baeshen R, Traorè SF, Diabate A, Tripet F - PLoS Genet. (2015)

Genomic structure of recombinant strains.The genomes of the assortatively-mating RbMM, RbSS and parental Mopti strains were compared using FST estimates at ~3x106 SNP marker loci (left Y-axis and red, blue and black lines). The genomic region introgressed from Kisumu into the Mopti genetic background and differing between the RbMM and RbSS recombinant strains is characterized by high FST values (blue shade) and extends from position ~14.5Mb to the centromere on chromosome X. The RbMM and RbSS differed at 160 protein-changing positions all of which located within the introgressed island and flanking region (right Y-axis, grey histogram bars). The pericentromeric region sharing conserved fixed differences with the field Anopheles coluzzii and gambiae s.s populations starts at position ~18.1Mb (orange shade). The position of inversions c, u and a on chromosome 2 is indicated (pink shade).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4400153&req=5

pgen.1005141.g002: Genomic structure of recombinant strains.The genomes of the assortatively-mating RbMM, RbSS and parental Mopti strains were compared using FST estimates at ~3x106 SNP marker loci (left Y-axis and red, blue and black lines). The genomic region introgressed from Kisumu into the Mopti genetic background and differing between the RbMM and RbSS recombinant strains is characterized by high FST values (blue shade) and extends from position ~14.5Mb to the centromere on chromosome X. The RbMM and RbSS differed at 160 protein-changing positions all of which located within the introgressed island and flanking region (right Y-axis, grey histogram bars). The pericentromeric region sharing conserved fixed differences with the field Anopheles coluzzii and gambiae s.s populations starts at position ~18.1Mb (orange shade). The position of inversions c, u and a on chromosome 2 is indicated (pink shade).
Mentions: The size of the X-island of divergence and flanking regions differing between the RbMM and RbSS strains was determined through genome-wide genetic differentiation (FST) scans and the occurrence of fixed coding differences between the recombinant strains. Estimates of genetic differentiation between the RbMM, RbSS and Mopti strains were calculated for 3,743,318 SNPs across the X, 2nd and 3rd chromosomes. The genome-wide FST scans showed that the RbSS differs from the RbMM and Mopti strains on chromosome X from the centromere to the reference position ~14.8Mb (Fig 2). This region covered the entire island of speciation plus a large flanking region. In addition, the RbSS and RbMM strain were genetically differentiated at a ~2Mb S-form fragment extending roughly from positions 11.5–13.5Mb (Fig 2). There were no other sizeable S-like regions detected through comparisons of the RbMM, RbSS and Mopti genomes, indicating that the selective introgression design worked as hoped for. Importantly, amongst all fixed differences observed between the RbMM and RbSS strains, non-synonymous differences inducing protein-coding changes (n = 160) were found only in the selectively-introgressed pericentromeric region (Fig 2). Fixed differences located elsewhere in the genome were either coding synonymous changes or non-coding.

Bottom Line: Furthermore, full-genome sequencing confirmed that protein-coding differences between recombinant strains were limited to the experimentally swapped pericentromeric region.Finally, targeted-genome comparisons showed that a number of these unique differences were conserved in sympatric field populations, thereby revealing candidate speciation genes.The functional demonstration of a close association between speciation genes and the X-island of differentiation lends unprecedented support to island-of-speciation models of sympatric speciation facilitated by pericentric recombination suppression.

View Article: PubMed Central - PubMed

Affiliation: Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, United Kingdom; Department of Animal Biology and Conservation Science, Faculty of Sciences, University of Ghana, Legon, Ghana.

ABSTRACT
Although many theoretical models of sympatric speciation propose that genes responsible for assortative mating amongst incipient species should be associated with genomic regions protected from recombination, there are few data to support this theory. The malaria mosquito, Anopheles gambiae, is known for its sympatric cryptic species maintained by pre-mating reproductive isolation and its putative genomic islands of speciation, and is therefore an ideal model system for studying the genomic signature associated with incipient sympatric speciation. Here we selectively introgressed the island of divergence located in the pericentric region of the X chromosome of An. gambiae s.s. into its sister taxon An. coluzzii through 5 generations of backcrossing followed by two generations of crosses within the introgressed strains that resulted in An. coluzzii-like recombinant strains fixed for the M and S marker in the X chromosome island. The mating preference of recombinant strains was then tested by giving virgin recombinant individuals a choice of mates with X-islands matching and non-matching their own island type. We show through genetic analyses of transferred sperm that recombinant females consistently mated with matching island-type males thereby associating assortative mating genes with the X-island of divergence. Furthermore, full-genome sequencing confirmed that protein-coding differences between recombinant strains were limited to the experimentally swapped pericentromeric region. Finally, targeted-genome comparisons showed that a number of these unique differences were conserved in sympatric field populations, thereby revealing candidate speciation genes. The functional demonstration of a close association between speciation genes and the X-island of differentiation lends unprecedented support to island-of-speciation models of sympatric speciation facilitated by pericentric recombination suppression.

No MeSH data available.


Related in: MedlinePlus