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.

Pre-copula acoustic behaviour of males in the malarial mosquitoes Anopheles coluzzii and Anopheles gambiae s.s. does not contribute to reproductive isolation

“…This could not only provide females with a mechanism for selecting high-quality males (Cator et al, 2010;Pennetier et al, 2010) but also play a role in the assortative mating of A. coluzzii and A. gambiae. Crucially, the hypothesis that assortative mating could be mediated by females is supported by the results of a recent study by Aboagye-Antwi et al (2015); behavioural assays in recombinant strains for the M and S markers in the X chromosome of both Anopheles species revealed that females, but not males, mated assortatively, indicating that a species recognition mechanism appears to be female dependent. This, however, does not mean that males do not contribute to assortative mating in nature; in the field, males are known to contribute to assortative mating via swarm spatial segregation (Diabaté et al, 2006;Dabiré et al, 2013;Sawadogo et al, 2013;Aboagye-Antwi et al, 2015).…”

A combination of sexual and ecological divergence contributes to rearrangement spread during initial stages of speciation

“…; Aboagye‐Antwi et al . ; Twyford & Friedman ). However, critically lacking is an understanding of the relative contributions of ecological divergence and assortative mating to rearrangement spread in populations.…”

“…A new inversion can also be favoured if it contains both a locus which contributes to assortative mating and a locus which contributes to hybrid inviability (Trickett & Butlin 1994;Dagilis & Kirkpatrick 2016). Empirical data support the presence of loci within rearrangements that contribute to sexual and ecologically important traits (Day & Butlin 1987;Lowry & Willis 2010;Ayala et al 2012;Andrew & Rieseberg 2013;Friedman & Willis 2013;Oneal et al 2014;Aboagye-Antwi et al 2015;Twyford & Friedman 2015). However, critically lacking is an understanding of the relative contributions of ecological divergence and assortative mating to rearrangement spread in populations.…”

Massive introgression drives species radiation at the range limit of Anopheles gambiae

“…Subsequent analyses have shown that divergence is more widespread around the genome than first thought517 and the involvement of two of the three islands of divergence in early-stage speciation became controversial5181920. However, a recent laboratory study has demonstrated that the chromosome-X island of divergence is associated with assortative mating between A. coluzzii and A. gambiae 21 confirming this genomic region as a primary candidate location for genes involved in reproductive isolation. These species have also shown differences in at least two genes which contribute to medically important phenotypes.…”