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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.

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Related in: MedlinePlus

Field population frequency distribution of protein coding SNPs identified in RbSS.A region covering the X-island and flanking region up to reference position 17Mbp was captured and re-sequenced in sympatric An. gambiae s.s. and An. coluzzii populations from Ghana. The frequency of alleles coding for unique protein differences in the RbSS recombinant strain was measured in the field An. gambiae s.s. population. The proportion of alleles occurring at high 0.8 (orange bars) and very high (freq >0.95: red bars) frequency increased towards the centromere suggesting a potential role in speciation whilst other alleles (blue bars) were not conserved (see text for details).
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pgen.1005141.g003: Field population frequency distribution of protein coding SNPs identified in RbSS.A region covering the X-island and flanking region up to reference position 17Mbp was captured and re-sequenced in sympatric An. gambiae s.s. and An. coluzzii populations from Ghana. The frequency of alleles coding for unique protein differences in the RbSS recombinant strain was measured in the field An. gambiae s.s. population. The proportion of alleles occurring at high 0.8 (orange bars) and very high (freq >0.95: red bars) frequency increased towards the centromere suggesting a potential role in speciation whilst other alleles (blue bars) were not conserved (see text for details).

Mentions: Given that the Kisumu and Mopti strains were colonized from allopatric populations over 25 and 7 years ago, some of the differences observed between the RbMM and RbSS strains could be due to genetic divergence of the original populations or result from genetic drift and inbreeding [34]. Consequently, we compared the protein-coding differences identified between RbMM and RbSS with those observed between 2 sympatric An. gambiae s.s. and An. coluzzii populations from Southern Ghana. Deep-pooled-targeted exon re-sequencing of the region extending from 17Mb to the centromere showed that, in 114 of the 117 coding differences distinguishing RbSS from RbMM, the M-form allele was fixed or nearly fixed (freq >0.95) in the field population of An. coluzzii. In the sympatric An. gambiae s.s., the alternate S-type allele was found at frequencies >0.8 in 61 of the 114 differences; and 20 of those were fixed or nearly fixed (freq >0.95) and thus conserved differences between sibling species. Conserved differences started from position ~18.1Mb (Fig 2), increased in frequency with proximity to the centromere and affected a total of 12 genes (Fig 3, Table 3).


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)

Field population frequency distribution of protein coding SNPs identified in RbSS.A region covering the X-island and flanking region up to reference position 17Mbp was captured and re-sequenced in sympatric An. gambiae s.s. and An. coluzzii populations from Ghana. The frequency of alleles coding for unique protein differences in the RbSS recombinant strain was measured in the field An. gambiae s.s. population. The proportion of alleles occurring at high 0.8 (orange bars) and very high (freq >0.95: red bars) frequency increased towards the centromere suggesting a potential role in speciation whilst other alleles (blue bars) were not conserved (see text for details).
© Copyright Policy
Related In: Results  -  Collection

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

pgen.1005141.g003: Field population frequency distribution of protein coding SNPs identified in RbSS.A region covering the X-island and flanking region up to reference position 17Mbp was captured and re-sequenced in sympatric An. gambiae s.s. and An. coluzzii populations from Ghana. The frequency of alleles coding for unique protein differences in the RbSS recombinant strain was measured in the field An. gambiae s.s. population. The proportion of alleles occurring at high 0.8 (orange bars) and very high (freq >0.95: red bars) frequency increased towards the centromere suggesting a potential role in speciation whilst other alleles (blue bars) were not conserved (see text for details).
Mentions: Given that the Kisumu and Mopti strains were colonized from allopatric populations over 25 and 7 years ago, some of the differences observed between the RbMM and RbSS strains could be due to genetic divergence of the original populations or result from genetic drift and inbreeding [34]. Consequently, we compared the protein-coding differences identified between RbMM and RbSS with those observed between 2 sympatric An. gambiae s.s. and An. coluzzii populations from Southern Ghana. Deep-pooled-targeted exon re-sequencing of the region extending from 17Mb to the centromere showed that, in 114 of the 117 coding differences distinguishing RbSS from RbMM, the M-form allele was fixed or nearly fixed (freq >0.95) in the field population of An. coluzzii. In the sympatric An. gambiae s.s., the alternate S-type allele was found at frequencies >0.8 in 61 of the 114 differences; and 20 of those were fixed or nearly fixed (freq >0.95) and thus conserved differences between sibling species. Conserved differences started from position ~18.1Mb (Fig 2), increased in frequency with proximity to the centromere and affected a total of 12 genes (Fig 3, Table 3).

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