title: Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation.
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.
authors.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.
authors.forename: Fred
authors.initials: F
authors.lastname: Aboagye-Antwi
authors.affiliation: Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, United Kingdom.
authors.forename: Nahla
authors.initials: N
authors.lastname: Alhafez
authors.affiliation: Centre for Genomic Research, University of Liverpool, Liverpool, United Kingdom.
authors.forename: Gareth D
authors.initials: GD
authors.lastname: Weedall
authors.affiliation: Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, United Kingdom.
authors.forename: Jessica
authors.initials: J
authors.lastname: Brothwood
authors.affiliation: Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, United Kingdom.
authors.forename: Sharanjit
authors.initials: S
authors.lastname: Kandola
authors.affiliation: Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, United Kingdom.
authors.forename: Doug
authors.initials: D
authors.lastname: Paton
authors.affiliation: Malaria Research and Training Center, Faculty of Medicine and Dentistry, University of Mali, Bamako, Mali.
authors.forename: Abrahamane
authors.initials: A
authors.lastname: Fofana
authors.affiliation: Centre for Genomic Research, University of Liverpool, Liverpool, United Kingdom.
authors.forename: Lisa
authors.initials: L
authors.lastname: Olohan
authors.affiliation: Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, United Kingdom.
authors.forename: Mauro Pazmiño
authors.initials: MP
authors.lastname: Betancourth
authors.affiliation: Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, United Kingdom.
authors.forename: Nkiru E
authors.initials: NE
authors.lastname: Ekechukwu
authors.affiliation: Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, United Kingdom.
authors.forename: Rowida
authors.initials: R
authors.lastname: Baeshen
authors.affiliation: Malaria Research and Training Center, Faculty of Medicine and Dentistry, University of Mali, Bamako, Mali.
authors.forename: Sékou F
authors.initials: SF
authors.lastname: Traorè
authors.affiliation: Institut de Recherche en Sciences de la Santé/Centre Muraz, Bobo-Dioulasso, Burkina Faso.
authors.forename: Abdoulaye
authors.initials: A
authors.lastname: Diabate
authors.affiliation: Centre for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, United Kingdom.
authors.forename: Frédéric
authors.initials: F
authors.lastname: Tripet
mesh_terms: D000818:Animals; D000852:Anopheles / Q000235:genetics* / Q000502:physiology; D059006:Chromosomes, Insect / Q000235:genetics*; D005260:Female; D049810:Genetic Speciation; D008297:Male; D052586:Mating Preference, Animal; D061350:Sympatry; D014960:X Chromosome / Q000235:genetics*