Experimental swap of Anopheles gambiae's assortative mating preferences demonstrates key role of X-chromosome divergence island in incipient sympatric speciation.

Fred Aboagye-Antwi,Gareth D Weedall,Abrahamane Fofana,Sékou F Traorè,Sharanjit Kandola,Abdoulaye Diabate,Nahla Alhafez,Frédéric Tripet,Nkiru E Ekechukwu,Rowida Baeshen,Doug Paton,Mauro Pazmiño Betancourth,Jessica Brothwood,Lisa Olohan,Bret A Payseur

doi:10.1371/journal.pgen.1005141

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.

Highlights

Unravelling the genomic processes underlying sympatric speciation, the evolution of new species from a single ancestral species within the same geographical region, is fundamental to our understanding of biodiversity
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
Theoretical studies predict that these islands, characterized by restricted genetic rearrangements, may protect genes of assortative mating between emerging species, and are fundamental to the speciation process

Summary

Introduction

Unravelling the genomic processes underlying sympatric speciation, the evolution of new species from a single ancestral species within the same geographical region, is fundamental to our understanding of biodiversity. At the core of this interest is the search for distinct genomic signatures that can help us understand what is thought to be a relatively narrow and unlikely set of genetic and ecological conditions facilitating the emergence and divergence of two gene pools from an originally panmictic population. Theoretical models of sympatric speciation have long recognised that this can only occur under a restricted set of conditions in which the genomic architecture often plays a major role [1,3,4]. Features of the genome such as chromosomal inversions and peri-centromeric regions that suppress recombination and link together genes of pre-mating isolation and ecological adaptation genes are predicted to facilitate sympatric speciation [1,5,6,7]. Hemizygosity and lower recombination rates are thought to predispose sex chromosomes to the more rapid accumulation of genes of pre and post-mating isolation [8]

Methods

Results

Discussion

Conclusion