No evidence for biased co-transmission of speciation islands inAnopheles gambiae

Abstract

Genome-scale scans have revealed highly heterogeneous levels of divergence between closely related taxa in many systems. Generally, a small number of regions show high differentiation, with the rest of the genome showing no or only low levels of divergence. These patterns have been interpreted as evidence for ongoing speciation-with-gene-flow, with introgression homogenizing the whole genome except loci involved in reproductive isolation. However, as the number of selected loci increases, the probability of introgression at unselected loci decreases unless there is a transmission ratio distortion causing an over-representation of specific combinations of alleles. Here we examine the transmission of three 'speciation islands' that contain fixed differences between the M and S forms of the mosquito, Anopheles gambiae. We made reciprocal crosses between M and S parents and genotyped over 2000 F 2 individuals, developing a hierarchical likelihood model to identify specific genotypes that are under-or over-represented among the recombinant offspring. Though our overall results did not match the expected number of F 2 genotypes, we found no biased co-transmission among M or S alleles in the three islands. Our likelihood model did identify transmission ratio distortion at two of the three islands, but this distortion was small (approx. 3%) and in opposite directions for the two islands. We discuss how our results impinge on hypotheses of current gene flow between M and S and ongoing speciation-with-gene-flow in this system.

Genomic divergence during speciation: causes and consequences

“…This point is exemplified in the empirical patterns described in this issue by Hahn et al [29] and the new theoretical results on expected coalescent patterns for neutral loci within chromosomal inversions reported by Guerrero et al [41]. Rather than casting despair, this simply highlights a clear avenue for further work.…”

“…These patterns quantified by 'genome scans' of numerous loci provide the empirical observations on which our current understanding of genomic divergence is based. Numerous studies in this issue present new empirical data or summarize the literature on how genetic differentiation is distributed throughout the genome [25][26][27][28][29][30][31][32][33]. The authors relate these patterns to the island metaphor to try and draw inferences concerning the significance of genome architecture and the processes facilitating speciation.…”

Spatiotemporal dynamics of gene flow and hybrid fitness between the M and S forms of the malaria mosquito, Anopheles gambiae

“…A few studies have used multiple restriction fragment length polymorphism assays and/or mismatch primer-based SNP assays to genotype one SNP in each of the three (X, 2L, and 3L) islands of divergence (26,36). We extended this approach with the development of the DIS assay (35) to describe A. gambiae populations throughout West Africa ( Fig.…”

“…White et al (26) reported nearly complete LD between the three islands of divergence in natural populations. Hahn et al (36) used laboratory crosses to demonstrate a lack of intrinsic incompatibilities that might explain this association. Based on these observations, it was proposed that the association among the three islands is maintained by near-complete RI between M and S forms in nature.…”

Genomic islands of divergence are not affected by geography of speciation in sunflowers

“…While there are reports of simpler genetic architectures of divergence, at least in some instances (especially early studies), scan resolution appears to have been too low to detect smaller islands of divergence (for example, Hahn et al 32 ).…”