The population genomics of trans-specific inversion polymorphisms in Anopheles gambiae

Abstract

In the malaria mosquito Anopheles gambiae polymorphic chromosomal inversions may play an important role in adaptation to environmental variation. Recently, we used microarray-based divergence mapping combined with targeted resequencing to map nucleotide differentiation between alternative arrangements of the 2La inversion. Here, we applied the same technique to four different polymorphic inversions on the 2R chromosome of An. gambiae. Surprisingly, divergence was much lower between alternative arrangements for all 2R inversions when compared to the 2La inversion. For one of the rearrangements, 2Ru, we successfully mapped a very small region (approximately 100 kb) of elevated divergence. For the other three rearrangements, we did not identify any regions of significantly high divergence, despite ample independent evidence from natural populations of geographic clines and seasonal cycling, and stable heterotic polymorphisms in laboratory populations. If these inversions are the targets of selection as hypothesized, we suggest that divergence between rearrangements may have escaped detection due to retained ancestral polymorphism in the case of the youngest 2R rearrangements and to extensive gene flux in the older 2R inversion systems that segregate in both An. gambiae and its sibling species An. arabiensis.

Figure 1.—

Sliding window analysis of divergence across the 2R chromosome between standard and inverted karyotypes, 2R+ vs. 2Rjbcu, measured in terms of proportion of SFPs per 300 probe window. Shaded areas represent chromosomal rearrangements. Horizontal dashed line is the significance threshold at 12 SFPs per window. A star denotes the significantly diverged genomic cluster in 2Ru. Beneath the plot are indicated the sequenced loci and their relative positions along chromosome 2R.

Figure 2.—

Comparison of nucleotide diversity (%) between standard (x-axis) and inverted (y-axis) arrangements for each of four polymorphic 2R inversions in An. gambiae. Each circle represents a gene sequenced in either the M form (open) or the S form (solid). Circles falling below the y-x line indicate reduced diversity in the inverted arrangement.

Figure 3.—

Nucleotide divergence between An. gambiae and An. arabiensis in chromosome 2 inversion systems. Pairwise nucleotide divergence per site (D_a) is averaged across the genes sequenced within each inversion system.

Figure 4.—

Model of chromosomal inversion history in the lineages leading to present-day An. arabiensis and An. gambiae populations. Proposed bidirectional or unidirectional introgression of arrangements between species is indicated by horizontal arrows (double headed or single headed, respectively).