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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

Percentage assortative mating in females and males carrying M or S-type X-chromosome islands.A) virgin females or males from the RbMM and RbSS recombinant strains where presented with a mixture of recombinant individuals of the opposite sex and with X-islands matching and non-matching their own X-island molecular type; B) virgin females or males from the M-form Mopti and S-form Kisumu strains used for creating the recombinant lines were given a choice between equal numbers of potential mates from both strains. The number and percentage of assortative and disassortative mating recorded across 3 replicates are indicated.
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pgen.1005141.g001: Percentage assortative mating in females and males carrying M or S-type X-chromosome islands.A) virgin females or males from the RbMM and RbSS recombinant strains where presented with a mixture of recombinant individuals of the opposite sex and with X-islands matching and non-matching their own X-island molecular type; B) virgin females or males from the M-form Mopti and S-form Kisumu strains used for creating the recombinant lines were given a choice between equal numbers of potential mates from both strains. The number and percentage of assortative and disassortative mating recorded across 3 replicates are indicated.

Mentions: Next, the mating choice preferences of females and males were tested using a standardized assortative mating assay (see methods). Reciprocal experiments were conducted in which virgin females or males from the same RbMM and RbSS cohorts were given a choice between mates with matching or non-matching X-island type (Table 2). Females from the RbMM were found to mate almost exclusively assortatively (Fig 1A)(P< 0.001). Females RbSS had their mating preferences effectively swapped and mated entirely with recombinant males with matching S-type islands (Fig 1A)(P< 0.001). In contrast, males from the RbMM and RbSS recombinant strains did not significantly prefer females with matching X-islands (P = 0.284 and 0.611 respectively). Since assortative mating amongst laboratory strains from An. coluzzii and An. gambiae s.s has never been reported, female and male choosiness were also assessed in the Mopti and Kisumu parental strains. Here again, females mated significantly assortatively (P< 0.001 in both strains) but not males (P = 0.073 and 0.163)(Fig 1B and S1 Table).


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)

Percentage assortative mating in females and males carrying M or S-type X-chromosome islands.A) virgin females or males from the RbMM and RbSS recombinant strains where presented with a mixture of recombinant individuals of the opposite sex and with X-islands matching and non-matching their own X-island molecular type; B) virgin females or males from the M-form Mopti and S-form Kisumu strains used for creating the recombinant lines were given a choice between equal numbers of potential mates from both strains. The number and percentage of assortative and disassortative mating recorded across 3 replicates are indicated.
© Copyright Policy
Related In: Results  -  Collection

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

pgen.1005141.g001: Percentage assortative mating in females and males carrying M or S-type X-chromosome islands.A) virgin females or males from the RbMM and RbSS recombinant strains where presented with a mixture of recombinant individuals of the opposite sex and with X-islands matching and non-matching their own X-island molecular type; B) virgin females or males from the M-form Mopti and S-form Kisumu strains used for creating the recombinant lines were given a choice between equal numbers of potential mates from both strains. The number and percentage of assortative and disassortative mating recorded across 3 replicates are indicated.
Mentions: Next, the mating choice preferences of females and males were tested using a standardized assortative mating assay (see methods). Reciprocal experiments were conducted in which virgin females or males from the same RbMM and RbSS cohorts were given a choice between mates with matching or non-matching X-island type (Table 2). Females from the RbMM were found to mate almost exclusively assortatively (Fig 1A)(P< 0.001). Females RbSS had their mating preferences effectively swapped and mated entirely with recombinant males with matching S-type islands (Fig 1A)(P< 0.001). In contrast, males from the RbMM and RbSS recombinant strains did not significantly prefer females with matching X-islands (P = 0.284 and 0.611 respectively). Since assortative mating amongst laboratory strains from An. coluzzii and An. gambiae s.s has never been reported, female and male choosiness were also assessed in the Mopti and Kisumu parental strains. Here again, females mated significantly assortatively (P< 0.001 in both strains) but not males (P = 0.073 and 0.163)(Fig 1B and S1 Table).

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