Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation.
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 know...
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doaj-cca8390c64a04cbc848987f281289f032020-11-24T21:41:57ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042015-04-01114e100514110.1371/journal.pgen.1005141Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation.Fred Aboagye-AntwiNahla AlhafezGareth D WeedallJessica BrothwoodSharanjit KandolaDoug PatonAbrahamane FofanaLisa OlohanMauro Pazmiño BetancourthNkiru E EkechukwuRowida BaeshenSékou F TraorèAbdoulaye DiabateFrédéric TripetAlthough 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.http://europepmc.org/articles/PMC4400153?pdf=render |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Fred Aboagye-Antwi Nahla Alhafez Gareth D Weedall Jessica Brothwood Sharanjit Kandola Doug Paton Abrahamane Fofana Lisa Olohan Mauro Pazmiño Betancourth Nkiru E Ekechukwu Rowida Baeshen Sékou F Traorè Abdoulaye Diabate Frédéric Tripet |
spellingShingle |
Fred Aboagye-Antwi Nahla Alhafez Gareth D Weedall Jessica Brothwood Sharanjit Kandola Doug Paton Abrahamane Fofana Lisa Olohan Mauro Pazmiño Betancourth Nkiru E Ekechukwu Rowida Baeshen Sékou F Traorè Abdoulaye Diabate Frédéric Tripet Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation. PLoS Genetics |
author_facet |
Fred Aboagye-Antwi Nahla Alhafez Gareth D Weedall Jessica Brothwood Sharanjit Kandola Doug Paton Abrahamane Fofana Lisa Olohan Mauro Pazmiño Betancourth Nkiru E Ekechukwu Rowida Baeshen Sékou F Traorè Abdoulaye Diabate Frédéric Tripet |
author_sort |
Fred Aboagye-Antwi |
title |
Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation. |
title_short |
Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation. |
title_full |
Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation. |
title_fullStr |
Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation. |
title_full_unstemmed |
Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation. |
title_sort |
experimental swap of anopheles gambiae's assortative mating preferences demonstrates key role of x-chromosome divergence island in incipient sympatric speciation. |
publisher |
Public Library of Science (PLoS) |
series |
PLoS Genetics |
issn |
1553-7390 1553-7404 |
publishDate |
2015-04-01 |
description |
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. |
url |
http://europepmc.org/articles/PMC4400153?pdf=render |
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