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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

Genetic crossing design used for selective introgression of the X-island of divergence in recombinant strains.Following the creation of hybrid females at the X-island diagnostic rDNA locus, 4 generations of backcrosses were used to introgress the S-type X-island into an M molecular form Mopti genetic background. Here, 'MM', 'MS' and 'SS' refer to the female genotypes at the rDNA marker locus in the X-island and 'M' and 'S' refers to the male genotype at the same locus (see methods). Thereafter 2 generations of crosses within the introgressed strain resulted in recombinants strains that shared a high genetic identity but differed at the S or M-type X-chromosome islands of divergence.
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pgen.1005141.g004: Genetic crossing design used for selective introgression of the X-island of divergence in recombinant strains.Following the creation of hybrid females at the X-island diagnostic rDNA locus, 4 generations of backcrosses were used to introgress the S-type X-island into an M molecular form Mopti genetic background. Here, 'MM', 'MS' and 'SS' refer to the female genotypes at the rDNA marker locus in the X-island and 'M' and 'S' refers to the male genotype at the same locus (see methods). Thereafter 2 generations of crosses within the introgressed strain resulted in recombinants strains that shared a high genetic identity but differed at the S or M-type X-chromosome islands of divergence.

Mentions: Hybrids between the two strains were created by crossing 100 M Mopti males with 100 SS Kisumu females (Fig 4). In order to obtain the 1st backcross progeny, 100 virgin MS hybrid females were mated with 100 virgin M Mopti males, resulting in male progeny of genotype M or S at the r-DNA locus and female of genotypes MM or MS (Fig 4). From generation 2 to 4, MS progeny females were backcrossed with M Mopti virgin males resulting in 4 generations of backcrossing (Fig 4). At each generation MS hybrid and MM families were obtained by bloodfeeding and setting up 80 females for individual oviposition. MS hybrid families were then distinguished from MM families by genotyping ten 2nd instar larvae reared in individual trays. The progenies of trays identified as containing MS hybrid larvae was pooled and reared under standard rearing conditions to obtain the next generation MS backcross females. Families identified as MM were discarded.


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)

Genetic crossing design used for selective introgression of the X-island of divergence in recombinant strains.Following the creation of hybrid females at the X-island diagnostic rDNA locus, 4 generations of backcrosses were used to introgress the S-type X-island into an M molecular form Mopti genetic background. Here, 'MM', 'MS' and 'SS' refer to the female genotypes at the rDNA marker locus in the X-island and 'M' and 'S' refers to the male genotype at the same locus (see methods). Thereafter 2 generations of crosses within the introgressed strain resulted in recombinants strains that shared a high genetic identity but differed at the S or M-type X-chromosome islands of divergence.
© Copyright Policy
Related In: Results  -  Collection

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

pgen.1005141.g004: Genetic crossing design used for selective introgression of the X-island of divergence in recombinant strains.Following the creation of hybrid females at the X-island diagnostic rDNA locus, 4 generations of backcrosses were used to introgress the S-type X-island into an M molecular form Mopti genetic background. Here, 'MM', 'MS' and 'SS' refer to the female genotypes at the rDNA marker locus in the X-island and 'M' and 'S' refers to the male genotype at the same locus (see methods). Thereafter 2 generations of crosses within the introgressed strain resulted in recombinants strains that shared a high genetic identity but differed at the S or M-type X-chromosome islands of divergence.
Mentions: Hybrids between the two strains were created by crossing 100 M Mopti males with 100 SS Kisumu females (Fig 4). In order to obtain the 1st backcross progeny, 100 virgin MS hybrid females were mated with 100 virgin M Mopti males, resulting in male progeny of genotype M or S at the r-DNA locus and female of genotypes MM or MS (Fig 4). From generation 2 to 4, MS progeny females were backcrossed with M Mopti virgin males resulting in 4 generations of backcrossing (Fig 4). At each generation MS hybrid and MM families were obtained by bloodfeeding and setting up 80 females for individual oviposition. MS hybrid families were then distinguished from MM families by genotyping ten 2nd instar larvae reared in individual trays. The progenies of trays identified as containing MS hybrid larvae was pooled and reared under standard rearing conditions to obtain the next generation MS backcross females. Families identified as MM were discarded.

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